Organization of the primate retina: electron microscopy

The retinae of monkey and man have been studied by electron microscopy to identify cell types, their processes and synaptic contacts. In the inner plexiform layer, the morphological characteristics of the three types of cells (bipolar, ganglion and amacrine) are described and seven synaptic relationships are identified. The bipolar terminals contain ribbons at points of synaptic contact, and, at these points, there are typically two postsynaptic processes, one a ganglion cell dendrite, the other an amacrine cell process. This synaptic arrangement is here termed a dyad. The amacrine cell processes themselves make synaptic contacts with ganglion cell dendrites and somata, other amacrine cell processes, and, most frequently, with the bipolar cell terminals. Often, the amacrine-bipolar contact is adjacent to a bipolar-amacrine junction, forming a reciprocal synaptic arrangement between the bipolar and the amacrine. In the more peripheral retina, large bipolar cell terminals (probably of rod bipolars) are occasionally observed adjacent to the perikarya of the ganglion cells. At these junctions, areas of fusion between the plasma membranes are seen, suggesting that such axosomatic junctions could be electrical. In the outer plexiform layer, synapses have been identified only in the receptor cell bases where receptor cells contact bipolar and horizontal cell processes. Synaptic contacts of the horizontal cells have not been clearly identified, but their strategic terminations in the receptor cell ending are described and interpreted as possibly synaptic. A model of the retina, based on the described anatomy, is presented and correlated with ganglion cell physiology.

1995 ◽  
Vol 12 (5) ◽  
pp. 919-927 ◽  
Author(s):  
Bao-Song Zhu ◽  
Ian Gibbins

AbstractSynaptic connections of amacrine cells with substance P-like or neuropeptide Y-like immunoreactivity (SP-LI or NPY-LI) in the retina of the cane toad, Bufo marinus, were investigated using ultrastructural immunocytochemistry. The perikarya of SP-LI or NPY-LI amacrine cells were located in the innermost row of the inner nuclear layer. The synapses associated with SP-LI amacrine cells were distributed mainly in sublaminae 3 and 4 with about 10% in sublamina 1 of the inner plexiform layer. The synapses formed by NPY-LI amacrine cells were found in sublaminae 1, 2, and 4 with approximately equal frequency. Of a total of 175 SP-LI profiles, 56% were in presynaptic positions and 44% in postsynaptic positions. The synaptic inputs to SP-LI profiles predominantly derived from other unlabeled amacrine cell dendrites, and to a lesser extent, from bipolar cell terminals. The majority of synaptic outputs from SP-LI amacrine cell dendrites were directed onto unlabeled amacrine cell processes. The SP-LI profiles also made synapses onto bipolar cell terminals and formed synapses onto presumed ganglion cell dendrites. Of a total of 200 NPY-LI profiles, 48% were in presynaptic positions and 52% in postsynaptic positions. The profiles of NPY-LI amacrine cells mainly received their synaptic inputs from other unlabeled amacrine cell processes, and to a lesser extent, from bipolar cell terminals. The majority of NPY-LI amacrine cell profiles gave their synaptic outputs onto unlabeled amacrine cell dendrites, and others formed synapses onto presumed ganglion cell processes. These results suggest that these two populations of neuropeptide-containing amacrine cells in the Bufo retina are involved in different synaptic circuits.


2002 ◽  
Vol 19 (3) ◽  
pp. 299-305 ◽  
Author(s):  
DAVID W. MARSHAK ◽  
ELIZABETH S. YAMADA ◽  
ANDREA S. BORDT ◽  
WENDY C. PERRYMAN

A labeled ON parasol ganglion cell from a macaque retina was analyzed in serial, ultrathin sections. It received 13% of its input from diffuse bipolar cells. These directed a large proportion of their output to amacrine cells but received a relatively small proportion of their amacrine cell input via feedback synapses. In these respects, they were similar to the DB3 bipolar cells that make synapses onto OFF parasol cells. Bipolar cell axons that contacted the ON parasol cell in stratum 4 of the inner plexiform layer always made synapses onto the dendrite, and therefore, the number of bipolar cell synapses onto these ganglion cells could be estimated reliably by light microscopy in the future. Amacrine cells provided the majority of inputs to the ON parasol cell. Only a few of the presynaptic amacrine cell processes received inputs from the same bipolar cells as the parasol cells, and most of the presynaptic amacrine cell processes did not receive any inputs at all within the series. These findings suggest that most of the inhibitory input to the ON parasol cell originates from other areas of the retina. Amacrine cells presynaptic to the parasol ganglion cell interacted very infrequently with other neurons in the circuit, and therefore, they would be expected to act independently, for the most part.


1993 ◽  
Vol 10 (3) ◽  
pp. 455-471 ◽  
Author(s):  
Lawrence B. Hurd ◽  
William D. Eldred

AbstractAlthough serotonin is thought to be a neurotransmitter in a number of retinal systems, much of the precise synaptic connectivity of serotonergic neurons is unknown. To address this issue, we used an antiserum directed against serotonin to label serotonergic bipolar and amacrine cells in the turtle retina. Light-microscopic analysis of labeled amacrine and bipolar cells indicated that both had bistratified dendritic arborizations primarily in stratum 1 and in strata 4/5 of the inner plexiform layer.Ultrastructural analysis of the neurocircuitry of these cells indicated that the processes of labeled bipolar cells in the outer plexiform layer made basal junction contacts with photoreceptor terminals. Only in rare instances did labeled bipolar cells processes invaginate near photoreceptor ribbon synapses. Processes of labeled bipolar cells received both conventional and small ribbon synaptic contacts in the outer plexiform layer. Bipolar cell processes in stratum 1 of the inner plexiform layer synapsed onto either amacrine/amacrine or amacrine/ganglion cell dyads, and made rare ribbon synaptic contacts onto labeled amacrine cell processes. Synaptic inputs to serotonergic bipolar cells in stratum 1 were from unlabeled bipolar and amacrine cells. Bipolar cell contacts in strata 4/5 were similar to those in stratum 1, but were fewer in number and no bipolar cell inputs were seen.Labeled amacrine cell output in both strata was onto other unlabeled amacrine cells and ganglion cells; but synaptic outputs to unlabeled bipolar cells were only seen in strata 4/5. In both strata 1 and 4/5, synaptic inputs to labeled amacrine cells were from both unlabeled amacrine cells and labeled bipolar cells. The serotonergic amacrine cells had many more synaptic interactions in stratum 1 than in strata 4/5 which supports the role of serotonergic bipolar cells in the OFF pathway of retinal processing. Interactions between serotonergic bipolar and amacrine cells may play an important role in visual processing.


2018 ◽  
Author(s):  
Robert E. Marc ◽  
Crystal Sigulinsky ◽  
Rebecca L. Pfeiffer ◽  
Daniel Emrich ◽  
James R. Anderson ◽  
...  

AbstractAll superclasses of retinal neurons display some form of electrical coupling including the key neurons of the inner plexiform layer: bipolar cells (BCs), amacrine or axonal cells (ACs) and ganglion cells (GCs). However, coupling varies extensively by class. For example, mammalian rod bipolar cells form no gap junctions at all, while all cone bipolar cells form class-specific coupling arrays, many of them homocellular in-superclass arrays. Ganglion cells are unique in that classes with coupling predominantly form heterocellular cross-class arrays of ganglion cell::amacrine cell (GC::AC) coupling in the mammalian retina. Ganglion cells are the least frequent superclass in the inner plexiform layer and GC::AC gap junctions are sparsely arrayed amidst massive cohorts of AC::AC, bipolar cell BC::BC, and AC::BC gap junctions. Many of these gap junctions and most ganglion cell gap junctions are suboptical, complicating analysis of specific ganglion cells. High resolution 2 nm TEM analysis of rabbit retinal connectome RC1 allows quantitative GC::AC coupling maps of identified ganglion cells. Ganglion cells classes apparently avoid direct cross-class homocellular coupling altogether even though they have opportunities via direct membrane touches, while transient OFF alpha ganglion cells and transient ON directionally selective (DS) ganglion cells are strongly coupled to distinct amacrine / axonal cell cohorts.A key feature of coupled ganglion cells is intercellular metabolite flux. Most GC::AC coupling involves GABAergic cells (γ+ amacrine cells), which results in significant GABA flux into ganglion cells. Surveying GABA coupling signatures in the ganglion cell layer across species suggests that the majority of vertebrate retinas engage in GC::AC coupling.Multi-hop synaptic queries of the entire RC1 connectome clearly profiles the coupled amacrine and axonal cells. Photic drive polarities and source bipolar cell class selec-tivities are tightly matched across coupled cells. OFF alpha ganglion cells are coupled to OFF γ+ amacrine cells and transient ON DS ganglion cells are coupled to ON γ+ amacrine cells including a large interstitial axonal cell (IAC). Synaptic tabulations show close matches between the classes of bipolar cells sampled by the coupled amacrine and ganglion cells. Further, both ON and OFF coupling ganglion networks show a common theme: synaptic asymmetry whereby the coupled γ+ neurons are also presynaptic to ganglion cell dendrites from different classes of ganglion cells outside the coupled set. In effect, these heterocellular coupling patterns enable an excited ganglion cell to directly inhibit nearby ganglion cells of different classes. Similarly, coupled γ+ amacrine cells engaged in feedback networks can leverage the additional gain of bipolar cell synapses in shaping the signaling of a spectrum of downstream targets based on their own selective coupling with ganglion cells.


2006 ◽  
Vol 23 (2) ◽  
pp. 221-231 ◽  
Author(s):  
MADHUMITA SEN ◽  
EVANNA GLEASON

We have examined the distribution of metabotropic glutamate receptors (mGluRs) 1 and 5 in the adult chicken retina using preembedding immuno-electronmicroscopy. Immunoreactivity for mGluRs 1 and 5 was found in both the outer plexiform layer (OPL) and the inner plexiform layer (IPL). For mGluR1, OPL labeling was observed at cone pedicles and horizontal and bipolar cell processes. In the IPL, mGluR1 labeling could be found on bipolar cell terminals, as well as postsynaptic processes, including amacrine cell processes. Neither presynaptic nor postsynaptic elements were labeled at rod synapses. For mGluR5, OPL labeling was associated with cone pedicles as well as bipolar and horizontal cell processes. As for mGluR1, rod synapses were unlabeled. In the IPL, labeling for mGluR5 was found on bipolar cell terminals and amacrine cell processes. The presynaptic expression of these receptors in the OPL was confirmed at the light level by double-labeling experiments with SV2. The distributions of mGluRs 1 and 5 indicate that they have the potential to regulate function in both synaptic layers. Furthermore, the similar expression patterns for these two receptors indicate that they might be co-expressed and thus have the potential to interact functionally.


1993 ◽  
Vol 10 (5) ◽  
pp. 907-914 ◽  
Author(s):  
Charles L. Zucker ◽  
Berndt Ehinger

AbstractThe distribution of glycine receptors in the turtle retina was studied with the aid of a monoclonal antibody that detects the 93-kD protein associated with the strychnine-sensitive glycine receptor. Light microscopically, receptors were found in the inner plexiform layer and, more sparsely, in the innermost parts of the inner nuclear layer. No receptors were seen to be associated with photoreceptor cells, horizontal cells, or any other structures in the distal inner nuclear layer or outer plexiform layer. Ultrastructurally, glycine receptors were found on the inner face of postsynaptic membranes of processes from amacrine and presumed ganglion cells and always involved amacrine cell processes as the presynaptic element. Such glycine receptor immunoreactive synapses onto amacrine cell processes were distributed throughout the inner plexiform layer with a peak density near the middle. On the other hand, output synapses onto ganglion cell processes displaying immunoreactive glycine receptor sites showed a bimodal distribution in the inner plexiform layer. Glycine receptor immunoreactivity was not detected on bipolar cells, but presumed glycine-utilizing processes (i.e. those presynaptic to immunoreactive glycine receptors) were occasionally found to be postsynaptic in bipolar cell dyads. The majority of the synaptic input to the presumed glycine-utilizing amacrine cell processes was from other amacrine processes, some of which were themselves glycine utilizing. The observations suggest that glycinergic synapses in the turtle retina are, to a large extent, engaged in processing interamacrine signals.


1997 ◽  
Vol 14 (6) ◽  
pp. 1089-1096 ◽  
Author(s):  
Bao-Song Zhu ◽  
Ian L. Gibbins

AbstractThe entire population of ganglion cells in the retina of the toad Bufo marinus was labeled by retrograde transport of a lysine-fixable biotinylated dextran amine of 3000 molecular weight. Synaptic connections between bipolar, amacrine, and ganglion cells in the inner plexiform layer were quantitatively analyzed, with emphasis on synaptic inputs to labeled ganglion cell dendrites. Synapses onto ganglion cell dendrites comprised 47% of a total of 1234 identified synapses in the inner plexiform layer. Approximately half of the bipolar or amacrine cell synapses were directed onto ganglion cell dendrites, while the rest were made mainly onto amacrine cell dendrites. Most of the synaptic inputs to ganglion cell dendrites derived from amacrine cell dendrites (84%), with the rest from bipolar cell terminals. Synaptic inputs to ganglion cell dendrites were distributed relatively uniformly throughout all sublaminae of the inner plexiform layer. The present study provides unambiguous identification of ganglion cell dendrites including very fine processes, enabling a detailed analysis of the types and distribution of synaptic inputs from the bipolar and amacrine cell to the ganglion cells. The retrograde tracing technique used in the present study will prove to be a useful tool for identifying synaptic inputs to ganglion cell dendrites from neurochemically identified bipolar and amacrine cell types in the retina.


2001 ◽  
Vol 18 (5) ◽  
pp. 741-751 ◽  
Author(s):  
P.T. JOHNSON ◽  
M.A. RAVEN ◽  
B.E. REESE

Photoreceptors in the ferret's retina have been shown to project transiently to the inner plexiform layer (IPL) prior to their differentiation of an outer segment. On postnatal day 15 (P-15), when this projection achieves maximal density, the photoreceptors projecting into the IPL extend primarily to one of two depths, coincident with the processes of cholinergic amacrine cells. The present study has used an excitotoxic approach employing subcutaneous injections of l-glutamate to ablate these cholinergic amacrine cells on P-7, in order to see whether their elimination alters this targeting of photoreceptor terminals within the IPL. The near-complete elimination of cholinergic amacrine cells at P-15 was confirmed, although the population of retinal ganglion cells was also affected, being depleted by roughly 50%. The rod opsin-immunopositive terminals in such treated ferrets no longer showed a stratified distribution, being found throughout the depth of the IPL, as well as extending into the ganglion cell layer. This effect should not be due to the partial loss of retinal ganglion cells, however, since optic nerve transection at P-2, which eliminates the ganglion cells entirely while leaving the cholinergic amacrine cell population intact, was shown not to affect the stratification pattern of the photoreceptors within the IPL. These results strongly suggest that the targeting of the photoreceptor terminals to discrete strata within the IPL is dependent upon the cholinergic amacrine cell processes.


2013 ◽  
Vol 31 (2) ◽  
pp. 153-163 ◽  
Author(s):  
KIYOHARU J. MIYAGISHIMA ◽  
ULRIKE GRÜNERT ◽  
WEI LI

AbstractColor information is encoded by two parallel pathways in the mammalian retina. One pathway compares signals from long- and middle-wavelength sensitive cones and generates red-green opponency. The other compares signals from short- and middle-/long-wavelength sensitive cones and generates blue-green (yellow) opponency. Whereas both pathways operate in trichromatic primates (including humans), the fundamental, phylogenetically ancient color mechanism shared among most mammals is blue-green opponency. In this review, we summarize the current understanding of how signals from short-wavelength sensitive cones are processed in the primate and nonprimate mammalian retina, with a focus on the inner plexiform layer where bipolar, amacrine, and ganglion cell processes interact to facilitate the generation of blue-green opponency.


1982 ◽  
Vol 214 (1196) ◽  
pp. 403-415 ◽  

Intracellular recordings were obtained from amacrine cells afterwards identified morphologically by horseradish peroxidase injection. There is a correlation between the time course of the photoresponses and the distribution of the cell processes across the inner plexiform layer (i. p. l.). Cells producing the shortest duration, transient ‘on‒off’ photoresponses branched in a single, narrow stratum of the i. p. l. (3‒7 μm across). Transient photoresponses with a longer time course were recorded from cells branching in a thicker stratum of i. p. l. (up to 20 μm), or from bistratified cells. Amacrine cells producing sustained centre-on or centre-off photoresponses were radially diffused across the whole i. p. l.; therefore this type of photoresponse need not be associated with a specific cellular stratification within the i. p. l. It is concluded that the two main functional types of amacrine cell, i. e. transient on‒off and sustained centre-on and centre-off, are subject to different structural organization of inputs than are the homologous physiological types of ganglion cells in this species, in the cat and in the carp. In a summary diagram the observed characteristics of the photoresponses are tentatively explained in term s of a non-homogeneous distribution of bipolar synaptic inputs along amacrine cell processes.


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